The Pho regulon and the pathogenesis of Escherichia coli

Veterinary Microbiology

Volumn 153, Issue 1-2, 2011, Pages 82-88

  Crépin, Sébastien ^a,b   Chekabab, Samuel Mohammed ^b   Le Bihan, Guillaume ^b   Bertrand, Nicolas ^b   Dozois, Charles M ^a,b   Harel, Josée ^b  

^a INRS INSTITUT ARMAND FRAPPIER   (Canada)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

Pathogenic Escherichia coli; Pho regulon; Stress response; Two component regulatory system

Indexed keywords

ADHESIN; PHOSPHATE; POLYPEPTIDE ANTIBIOTIC AGENT; VIRULENCE FACTOR;

BACTERIAL CELL; BACTERIAL STRAIN; CELL SURFACE; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTION; GENE FUNCTION; HOMEOSTASIS; HOST CELL; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PHO REGULON; REGULON; REVIEW; VIRULENCE;

BACTERIAL PROTEINS; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; PHOSPHATES; REGULON; TRANSCRIPTION, GENETIC; VIRULENCE;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 80052529234     PISSN: 03781135     EISSN: 18732542     Source Type: Journal    
DOI: 10.1016/j.vetmic.2011.05.043     Document Type: Review

References (63)

1. Allen K.J., Lepp D., McKellar R.C., Griffiths M.W. Examination of stress and virulence gene expression in Escherichia coli O157:H7 using targeted microarray analysis. Foodborne Pathog. Dis. 2008, 5:437-447.
2. Baek J.H., Lee S.Y. Novel gene members in the Pho regulon of Escherichia coli. FEMS Microbiol. Lett. 2006, 264:104-109.
3. Baek J.H., Lee S.Y. Transcriptome analysis of phosphate starvation response in Escherichia coli. J. Microbiol. Biotechol. 2007, 17:244-252.
4. Bahrani-Mougeot F.K., Buckles E.L., Lockatell C.V., Hebel J.R., Johnson D.E., Tang C.M., Donnenberg M.S. Type 1 fimbriae and extracellular polysaccharides are preeminent uropathogenic Escherichia coli virulence determinants in the murine urinary tract. Mol. Microbiol. 2002, 45:1079-1093.
5. Barnes H.J., Vaillancourt J.-P., Gross W.B. Colibacillosis. Diseases of Poultry 2003, 631-652. Iowa State Press, Ames, Iowa. 11th ed. Y.M. Saif, H.J. Barnes, J.R. Glisson, A.M. Fadly, L.R. McDougald, D.E. Swayne (Eds.).
6. Batisson I., Guimond M.P., Girard F., An H., Zhu C., Oswald E., Fairbrother J.M., Jacques M., Harel J. Characterization of the novel factor paa involved in the early steps of the adhesion mechanism of attaching and effacing Escherichia coli. Infect. Immun. 2003, 71:4516-4525.
7. Belanger L., Garenaux A., Harel J., Boulianne M., Nadeau E., Dozois C.M. Escherichia coli from animal reservoirs as a potential source of human extraintestinal pathogenic E. coli. FEMS Immunol. Med. Microbiol. 2011, 62:1-10.
8. Bertrand N., Houle S., Lebihan G., Poirier E., Dozois C.M., Harel J. Increased Pho regulon activation correlates with decreased virulence of an avian pathogenic Escherichia coli O78 strain. Infect. Immun. 2010, 78:5324-5331.
9. Bhatt K., Banerjee S.K., Chakraborti P.K. Evidence that phosphate specific transporter is amplified in a fluoroquinolone resistant Mycobacterium smegmatis. Eur. J. Biochem. - FEBS 2000, 267:4028-4032.
10. Bishop R.E. Fundamentals of endotoxin structure and function. Contrib. Microbiol. 2005, 12:1-27.
11. Cegelski L., Marshall G.R., Eldridge G.R., Hultgren S.J. The biology and future prospects of antivirulence therapies. Nat. Rev. Microbiol. 2008, 6:17-27.
12. Cegelski L., Pinkner J.S., Hammer N.D., Cusumano C.K., Hung C.S., Chorell E., Aberg V., Walker J.N., Seed P.C., Almqvist F., Chapman M.R., Hultgren S.J. Small-molecule inhibitors target Escherichia coli amyloid biogenesis and biofilm formation. Nat. Chem. Biol. 2009, 5:913-919.
13. Chauhan N., Calderone R. Two-component signal transduction proteins as potential drug targets in medically important fungi. Infect. Immun. 2008, 76:4795-4803.
14. Cheng C., Tennant S.M., Azzopardi K.I., Bennett-Wood V., Hartland E.L., Robins-Browne R.M., Tauschek M. Contribution of the pst-phoU operon to cell adherence by atypical enteropathogenic Escherichia coli and virulence of Citrobacter rodentium. Infect. Immun. 2009, 77:1936-1944.
15. Connell I., Agace W., Klemm P., Schembri M., Marild S., Svanborg C. Type 1 fimbrial expression enhances Escherichia coli virulence for the urinary tract. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:9827-9832.
16. Crepin S., Lamarche M.G., Garneau P., Seguin J., Proulx J., Dozois C.M., Harel J. Genome-wide transcriptional response of an avian pathogenic Escherichia coli (APEC) pst mutant. BMC Genomics 2008, 9:568.
17. Critzer F.J., D'Souza D.H., Saxton A.M., Golden D.A. Increased transcription of the phosphate-specific transport system of Escherichia coli O157:H7 after exposure to sodium benzoate. J. Food Prot. 2010, 73:819-824.
18. Daigle F., Fairbrother J.M., Harel J. Identification of a mutation in the pst-phoU operon that reduces pathogenicity of an Escherichia coli strain causing septicemia in pigs. Infect. Immun. 1995, 63:4924-4927.
19. Dobrindt U., Hacker J. Targeting virulence traits: potential strategies to combat extraintestinal pathogenic E. coli infections. Curr. Opin. Microbiol. 2008, 11:409-413.
20. Dozois C.M., Chanteloup N., Dho-Moulin M., Bree A., Desautels C., Fairbrother J.M. Bacterial colonization and in vivo expression of F1 (type 1) fimbrial antigens in chickens experimentally infected with pathogenic Escherichia coli. Avian Dis. 1994, 38:231-239.
21. Dozois C.M., Daigle F., Curtiss R. Identification of pathogen-specific and conserved genes expressed in vivo by an avian pathogenic Escherichia coli strain. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:247-252.
22. Dziva F., van Diemen P.M., Stevens M.P., Smith A.J., Wallis T.S. Identification of Escherichia coli O157:H7 genes influencing colonization of the bovine gastrointestinal tract using signature-tagged mutagenesis. Microbiology 2004, 150:3631-3645.
23. Ferreira G.M., Spira B. The pst operon of enteropathogenic Escherichia coli enhances bacterial adherence to epithelial cells. Microbiology 2008, 154:2025-2036.
24. Frirdich E., Whitfield C. Lipopolysaccharide inner core oligosaccharide structure and outer membrane stability in human pathogens belonging to the Enterobacteriaceae. J. Endotoxin Res. 2005, 11:133-144.
25. Gao R., Stock A.M. Biological insights from structures of two-component proteins. Annu. Rev. Microbiol. 2009, 63:133-154.
26. Garrity-Ryan L.K., Kim O.K., Balada-Llasat J.M., Bartlett V.J., Verma A.K., Fisher M.L., Castillo C., Songsungthong W., Tanaka S.K., Levy S.B., Mecsas J., Alekshun M.N. Small molecule inhibitors of LcrF, a Yersinia pseudotuberculosis transcription factor, attenuate virulence and limit infection in a murine pneumonia model. Infect. Immun. 2010, 78:4683-4690.
27. Hsieh Y.J., Wanner B.L. Global regulation by the seven-component Pi signaling system. Curr. Opin. Microbiol. 2010, 13:198-203.
28. Jacobsen S.M., Lane M.C., Harro J.M., Shirtliff M.E., Mobley H.L. The high-affinity phosphate transporter Pst is a virulence factor for Proteus mirabilis during complicated urinary tract infection. FEMS Immunol. Med. Microbiol. 2008, 52:180-193.
29. John M., Kudva I.T., Griffin R.W., Dodson A.W., McManus B., Krastins B., Sarracino D., Progulske-Fox A., Hillman J.D., Handfield M., Tarr P.I., Calderwood S.B. Use of in vivo-induced antigen technology for identification of Escherichia coli O157:H7 proteins expressed during human infection. Infect. Immun. 2005, 73:2665-2679.
30. Johnson J.R., Clabots C., Rosen H. Effect of inactivation of the global oxidative stress regulator oxyR on the colonization ability of Escherichia coli O1:K1:H7 in a mouse model of ascending urinary tract infection. Infect. Immun. 2006, 74:461-468.
31. Kaper J.B., Nataro J.P., Mobley H.L. Pathogenic Escherichia coli. Nat. Rev. Microbiol. 2004, 2:123-140.
32. Kim Y., Oh S., Park S., Kim S.H. Interactive transcriptome analysis of enterohemorrhagic Escherichia coli (EHEC) O157:H7 and intestinal epithelial HT-29 cells after bacterial attachment. Int. J. Food Microbiol. 2009, 131:224-232.
33. Lamarche M.G., Harel J. Membrane homeostasis requires intact pst in extraintestinal pathogenic Escherichia coli. Curr. Microbiol. 2010, 60:356-359.
34. Lamarche M.G., Dozois C.M., Daigle F., Caza M., Curtiss R., Dubreuil J.D., Harel J. Inactivation of the pst system reduces the virulence of an avian pathogenic Escherichia coli O78 strain. Infect. Immun. 2005, 73:4138-4145.
35. Lamarche M.G., Kim S.H., Crepin S., Mourez M., Bertrand N., Bishop R.E., Dubreuil J.D., Harel J. Modulation of hexa-acyl pyrophosphate lipid A population under Escherichia coli phosphate (Pho) regulon activation. J. Bacteriol. 2008, 190:5256-5264.
36. Lamarche M.G., Wanner B.L., Crepin S., Harel J. The phosphate regulon and bacterial virulence: a regulatory network connecting phosphate homeostasis and pathogenesis. FEMS Microbiol. Rev. 2008, 32:461-473.
37. Mattmann M.E., Blackwell H.E. Small molecules that modulate quorum sensing and control virulence in Pseudomonas aeruginosa. J. Org. Chem. 2010, 75:6737-6746.
38. Mizuno T. Compilation of all genes encoding two-component phosphotransfer signal transducers in the genome of Escherichia coli. DNA Res. 1997, 4:161-168.
39. Moreau P.L The lysine decarboxylase CadA protects Escherichia coli starved of phosphate against fermentation acids. J. Bacteriol. 2007, 189:2249-2261.
40. Moreau P.L., Gerard F., Lutz N.W., Cozzone P. Non-growing Escherichia coli cells starved for glucose or phosphate use different mechanisms to survive oxidative stress. Mol. Microbiol. 2001, 39:1048-1060.
41. Mulvey M.A., Lopez-Boado Y.S., Wilson C.L., Roth R., Parks W.C., Heuser J., Hultgren S.J. Induction and evasion of host defenses by type 1-piliated uropathogenic Escherichia coli. Science 1998, 282:1494-1497.
42. Ngeleka M., Harel J., Jacques M., Fairbrother J.M. Characterization of a polysaccharide capsular antigen of septicemic Escherichia coli O115:K " V165" :F165 and evaluation of its role in pathogenicity. Infect. Immun. 1992, 60:5048-5056.
43. Nielubowicz G.R., Mobley H.L. Host-pathogen interactions in urinary tract infection. Nat. Rev. Urol. 2010, 7:430-441.
44. Nikaido H. Molecular basis of bacterial outer membrane permeability revisited. Microbiol. Mol. Biol. Rev. 2003, 67:593-656.
45. Nikaido H., Vaara M. Molecular basis of bacterial outer membrane permeability. Microbiol. Rev. 1985, 49:1-32.
46. Pourbakhsh S.A., Boulianne M., Martineau-Doize B., Dozois C.M., Desautels C., Fairbrother J.M. Dynamics of Escherichia coli infection in experimentally inoculated chickens. Avian Dis. 1997, 41:221-233.
47. Pratt J.T., Ismail A.M., Camilli A. PhoB regulates both environmental and virulence gene expression in Vibrio cholerae. Mol. Microbiol. 2010, 77:1595-1605.
48. Rasko D.A., Moreira C.G., Li de R., Reading N.C., Ritchie J.M., Waldor M.K., Williams N., Taussig R., Wei S., Roth M., Hughes D.T., Huntley J.F., Fina M.W., Falck J.R., Sperandio V. Targeting QseC signaling and virulence for antibiotic development. Science 2008, 321:1078-1080.
49. Ron E.Z. Host specificity of septicemic Escherichia coli: human and avian pathogens. Curr. Opin. Microbiol. 2006, 9:28-32.
50. Schaeffer A.J., Schwan W.R., Hultgren S.J., Duncan J.L. Relationship of type 1 pilus expression in Escherichia coli to ascending urinary tract infections in mice. Infect. Immun. 1987, 55:373-380.
51. Seib K.L., Wu H.J., Kidd S.P., Apicella M.A., Jennings M.P., McEwan A.G. Defenses against oxidative stress in Neisseria gonorrhoeae: a system tailored for a challenging environment. Microbiol. Mol. Biol. Rev. 2006, 70:344-361.
52. Snyder J.A., Haugen B.J., Buckles E.L., Lockatell C.V., Johnson D.E., Donnenberg M.S., Welch R.A., Mobley H.L. Transcriptome of uropathogenic Escherichia coli during urinary tract infection. Infect. Immun. 2004, 72:6373-6381.
53. Suziedeliene E., Suziedelis K., Garbenciute V., Normark S. The acid-inducible asr gene in Escherichia coli: transcriptional control by the phoBR operon. J. Bacteriol. 1999, 181:2084-2093.
54. Taschner N.P., Yagil E., Spira B. A differential effect of σs on the expression of the PHO regulon genes of Escherichia coli. Microbiology 2004, 150:2985-2992.
55. Teng C.H., Cai M., Shin S., Xie Y., Kim K.J., Khan N.A., Di Cello F., Kim K.S. Escherichia coli K1 RS218 interacts with human brain microvascular endothelial cells via type 1 fimbria bacteria in the fimbriated state. Infect. Immun. 2005, 73:2923-2931.
56. VanBogelen R.A., Olson E.R., Wanner B.L., Neidhardt F.C. Global analysis of proteins synthesized during phosphorus restriction in Escherichia coli. J. Bacteriol. 1996, 178:4344-4366.
57. van Diemen P.M., Dziva F., Stevens M.P., Wallis T.S. Identification of enterohemorrhagic Escherichia coli O26:H-genes required for intestinal colonization in calves. Infect. Immun. 2005, 73:1735-1743.
58. Wang S., Deng K., Zaremba S., Deng X., Lin C., Wang Q., Tortorello M.L., Zhang W. Transcriptomic response of Escherichia coli O157:H7 to oxidative stress. Appl. Environ. Microbiol. 2009, 75:6110-6123.
59. Wanner B.L. Phosphorus assimilation and control of the phosphate regulon. Escherichia coli and Salmonella: Cellular and Molecular Biology 1996, vol. 1:1357-1381. American Society for Microbiology, Washington, DC.
60. West A.H., Stock A.M. Histidine kinases and response regulator proteins in two-component signaling systems. Trends Biochem. Sci. 2001, 26:369-376.
61. Yoshida Y., Sugiyama S., Oyamada T., Yokoyama K., Makino K. Identification and characterization of novel phosphate regulon genes, ecs0540-ecs0544, in Escherichia coli O157:H7. Mol. Genet. Gen. 2010, 284:197-205.
62. Yuan Z.C., Zaheer R., Morton R., Finan T.M. Genome prediction of PhoB regulated promoters in Sinorhizobium meliloti and twelve proteobacteria. Nucleic Acids Res. 2006, 34:2686-2697.
63. Zavaleta-Pastor M., Sohlenkamp C., Gao J.L., Guan Z., Zaheer R., Finan T.M., Raetz C.R., Lopez-Lara I.M., Geiger O. Sinorhizobium meliloti phospholipase C required for lipid remodeling during phosphorus limitation. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:302-307.